Article pubs.acs.org/JPCB
AH Peptide-Mediated Formation of Charged Planar Lipid Bilayers Goh Haw Zan,†,‡ Joshua A. Jackman,†,‡ and Nam-Joon Cho*,†,‡,§ †
School of Materials Science and Engineering, Nanyang Technological University, 50 Nanyang Avenue 639798, Singapore Centre for Biomimetic Sensor Science, Nanyang Technological University, 50 Nanyang Drive 637553, Singapore § School of Chemical and Biomedical Engineering, Nanyang Technological University, 62 Nanyang Drive 637459, Singapore ‡
S Supporting Information *
ABSTRACT: Planar lipid bilayers on solid supports provide a controllable platform to mimic biological membranes. Adsorption and spontaneous rupture of vesicles is the most common method to form planar bilayers. While many substrates support vesicle adsorption, vesicles rupture spontaneously on only a few materials. In order to form planar bilayers on materials intractable to conventional vesicle fusion, an amphipathic, α-helical (AH) peptide has been identified that can rupture adsorbed vesicles and form planar bilayers on previously intractable materials. Most studies using AH peptide have employed zwitterionic lipid compositions only, and the range of suitable lipid compositions remains to be elucidated. Herein, using quartz crystal microbalance-dissipation and ellipsometry, we investigated the effects of membrane surface charge on AH peptide-mediated bilayer formation via the rupture of surface-adsorbed vesicles on titanium oxide. Our findings demonstrate that AH peptide can promote the formation of positively and negatively charged bilayers. Importantly, the kinetics of vesicle rupture by AH peptide are strongly influenced by the membrane surface charge. Although the titanium oxide surface is negatively charged, the formation of negatively charged bilayers was quickest among the tested lipid compositions. Taken together, the experimental data supports that the effects of membrane surface charge on the rupture kinetics are related to variations in the extent of vesicle destabilization prior to vesicle rupture. Given the wide range of lipid compositions amenable to AH peptidemediated vesicle rupture, this work further suggests that AH peptide is largely unique among membrane-active peptides, thereby substantiating its position as a promising broad-spectrum antiviral agent.
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INTRODUCTION The planar lipid bilayer is a widely studied, two-dimensional cell membrane mimic that can form on solid supports.1 Owing to its high electrical sealing and amenability to characterization by a wide range of surface-sensitve techniques,2 several design strategies have been developed to fabricate planar bilayers. The primary method is vesicle fusion, which involves the adsorption and spontaneous rupture of lipid vesicles on hydrophilic solid supports.3 However, the range of surfaces is limited to mainly silaceous materials, including silicon oxide4 and mica.5 In order to form a planar bilayer of desired composition, process optimization is possible based on adjusting vesicle properties (e.g., size, lamellarity) and experimental conditions (e.g., ionic strength, solution pH, osmotic pressure, and temperature) (see refs 3, 6, 7, and references therein). Depending on the case, optimization can be nontrivial, and alternative methods that employ a standardized protocol are desirable for widespread utility. One of the main goals in the field is to identify a suitable method that permits large-scale fabrication of a planar bilayer on different solid supports.8 Despite its advantages, vesicle fusion requires an appreciably higher adhesion energy than that required for supporting a planar bilayer.9 On many substrates, including gold,4 titanium oxide,10 and aluminum oxide,9 the adhesion energy is sufficient for vesicle adsorption, but not for spontaneous rupture, and vesicles instead remain intact. © 2014 American Chemical Society
Nevertheless, based on the lipid−substrate interaction, it is thermodynamically favorable to support planar bilayers on these substrates. The main challenge is to identify a method other than vesicle fusion that promotes vesicle rupture in such cases. To this end, an amphipathic, α-helical (AH) peptide was identified that can rupture surface-adsorbed vesicles.11 AH peptide is derived from the N-terminal amphipathic helix of the hepatitis C virus (HCV) NS5A protein, which is necessary for membrane association related to HCV genome replication.12 In the course of studying HCV replication, it was serendipitously discovered that the isolated AH peptide also has an additional function, namely, the capability to rupture lipid vesicles as well as certain types of enveloped viruses.11,13 When applied to an adsorbed vesicle layer on gold or titanium oxide, AH peptide causes vesicle rupture, which leads to planar bilayer formation.14 The vesicle-to-bilayer structural transformation occurs because AH peptide causes vesicle destabilization that leads to vesicle fusion and eventually rupture.15,16 Practically, vesicle rupture occurs only for small vesicles so it is necessary to use appropriatesize vesicles (preferably less than 100 nm diameter) for AH peptide-mediated bilayer formation.13 Received: November 27, 2013 Revised: January 30, 2014 Published: March 14, 2014 3616
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Method of Cumulants in order to calculate the intensityweighted Gaussian profile of each vesicle size distribution, including average effective diameter and polydispersity. Quartz Crystal Microbalance-Dissipation (QCM-D). QCM-D experiments were performed on a Q-Sense E4 instrument (Q-Sense AB, Gothenburg, Sweden). Experimental data were collected at several overtones (n = 3, 5, 7, 9), and changes in resonance frequency and energy dissipation were monitored as functions of time. Unless otherwise noted, the data presented was collected at the third overtone. For viscoelastic modeling, measurement data from the third to ninth overtones were fit to the Voigt-Voinova model in order to recover the effective Voigt thickness, shear modulus, and viscosity of the adlayer.22 A constant film density of 1000 kg·m−3 was assumed, and the results are consistent with previous related work.11,13,15,21,23 Ellipsometry. A Nanofilm EP3 ellipsometer (Accurion GmbH, Germany) was used for optical measurement at incident and reflected angles of 65°. Ellipsometric measurements were controlled with the EP3View software (Accurion GmbH). The Nanofilm EP3 ellipsometer employs a PCSA configuration in order to determine the rotation angles of the polarizer and analyzer that lead to nulling conditions for retrieving Δ and Ψ. Incident light with a wavelength of 545.6 nm was selected from a Xenon lamp by using an interference filter. The measured Δ and Ψ were fit to a layered structure in order to obtain the complex refractive index and thickness of each layer by using the EP4 model software (Accurion GmbH). To obtain the optical and structural properties of the substrates, measurements were carried out in air, buffer, and ethanol as ambient conditions. As the titanium oxide coating was sufficiently thick to render the surfaces opaque, the titanium was treated as a semi-infinite thickness layer and the substrates were modeled as a Ti/TiO2/ ambient multilayer. Additionally, the absorbed lipid vesicles or planar bilayer deposited on the substrate was modeled as a homogeneous layer with a refractive index n and a thickness d.24 n was constrained from 1.336 (refractive index of buffer) to 1.5 (refractive index of a lipid bilayer), and d was constrained from 0 to 100 nm. Subsequently, the optical mass of the layer, Δmoptical, was obtained from nlayer and dlayer by using the de Feijter25 formula with a dn/dc value of 0.14 mL·g−1 for the refractive index increment.
While most studies related to AH peptide have used zwitterionic lipid compositions, Hardy et al. demonstrated that AH peptide can also rupture vesicles that contain a more biologically relevant mixture of phospholipids, sphingolipids, and cholesterol.17 This finding is important because it demonstrated that AH peptide can promote vesicle rupture not only in cases of weak adhesion energy, but also in cases where vesicles have high bending rigidity. Thus, AH peptide has the potential to serve as an external agent to promote vesicle rupture in more general terms. In this work, we have investigated the effects of membrane surface charge on AH peptide-mediated vesicle rupture to form planar bilayers. From a design perspective, membrane surface charge is an important experimental parameter for model membrane fabrication. Cellular membranes are generally negatively charged or zwitterionic,18 while vesicle drug delivery systems can be positively charged.19 Hence, developing a strategy to form planar bilayers with different lipid compositions on formerly intractable substrates (e.g., titanium oxide) provides flexibility to mimic various kinds of lipid membrane systems for fundamental and applied investigations.
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MATERIALS AND METHODS Experimental Substrates. All measurements were performed on titanium oxide-coated sensor crystals (Q-Sense AB, Gothenburg, Sweden). The substrates were cleaned with 1% w/ w sodium dodecyl sulfate (SDS) solution, and then rinsed with water and ethanol, sequentially. After gentle drying with a stream of nitrogen air, the crystals were subjected to oxygen plasma treatment (Harrick Plasma, Ithaca, NY, USA) for ∼1 min immediately before experiment. Vesicle Preparation. 1-Palmitoyl-2-oleoyl-sn-glycero-3phosphocholine (POPC), 1-palmitoyl-2-oleoyl-sn-glycero-3phospho-L-serine (sodium salt) (POPS), and 1-palmitoyl-2oleoyl-sn-glycero-3-ethylphosphocholine (chloride salt) (POEPC) were used as-supplied in chloroform from Avanti Polar Lipids (Alabaster, AL, USA). Small unilamellar vesicles of desired lipid composition were prepared at a lipid concentration of 5 mg·mL−1 by the extrusion method, as previously described.20 Vesicles were extruded by using a Mini Extruder (Avanti Polar Lipids) through track-etched polycarbonate membranes with 50nm-diameter pores and then again with 30-nm-diameter pores. The z-average diameter of extruded vesicles was less than 60 nm with a polydispersity index of less than 0.1, as measured by dynamic light scattering. Vesicles were diluted before experiment, and were used within 2 days of preparation. An aqueous buffer solution of 200 mM NaCl and 10 mM Tris [pH 7] was used in all experiments. All buffers and solutions were prepared with 18.2 MΩ·cm Milli-Q water (MilliPore, Oregon, USA). Peptides. AH peptide was synthesized by Anaspec Corporation (San Jose, CA, USA). The sequence of AH peptide is H-Ser-Gly-Ser-Trp-Leu-Arg-Asp-Val-Trp-Asp-Trp-Ile-CysThr-Val-Leu-Thr-Asp-Phe-Lys-Thr-Trp-Leu-Gln-Ser-Lys-LeuAsp-Tyr-Lys-Asp-NH2. The peptide concentration was 13 μM for all experiments in this study based on previous work11,13,15,17,21 that reported vesicle rupture in this peptide concentration range (13−15 μM). Dynamic Light Scattering. Dynamic light scattering (DLS) experiments were performed on a 90Plus Particle Size Analyzer with a 658.0 nm monochromatic laser (Brookhaven Instruments Corporation, New York, USA). All measurements were taken at a scattering angle of 90° where the reflection effect is minimized. All autocorrelation functions obtained were deconvoluted by the
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RESULTS AND DISCUSSION In order to investigate the effects of membrane surface charge on AH peptide-mediated bilayer formation, we first prepared extruded vesicles containing zwitterionic POPC lipid along with up to 30 mol % positively charged POEPC lipid or negatively charged POPS lipid. The average diameter of extruded vesicles was below 60 nm, as measured by dynamic light scattering. The vesicle size distributions were well within the targeting range of AH peptide.13 After vesicle preparation, the vesicles were added to a titanium oxide substrate and the adsorption kinetics were tracked by QCM-D monitoring (Figure 1, Arrow 1). In all cases, an adsorbed vesicle layer was formed based on changes in frequency and energy dissipation of approximately −100 to −120 Hz and (4 to 6) × 10−6, respectively. To attempt planar bilayer formation, AH peptide was then added to the adsorbed vesicle layer (Figure 1, Arrow 2). Independent of lipid composition, the AH peptide binding interaction was initially observed until reaching a maximum decrease in frequency, as denoted by an inflection point (Figures 3617
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Table 1. Summary Table for AH Peptide-Mediated Planar Bilayer Formationa lipid composition
Δfrequencyn=3/3 (Hz)
Δdissipationn=3 (10‑6)
POPC:POEPC 70:30 POPC:POEPC 85:15 POPC POPC:POPS 85:15 POPC:POPS 70:30
26.8 ± 1.0 27.4 ± 1.1 26.5 ± 0.4 24.8 ± 2.9 23.6 ± 1.1
0.08 ± 0.10 0.13 ± 0.10 0.07 ± 0.06 0.24 ± 0.53 0.09 ± 0.07
a
Final changes in frequency and energy dissipation are reported as a function of lipid composition, as monitored by the QCM-D measurement technique. Each reported value is the average ± standard deviation of several measurements (at least n = 3).
To analyze the dependence of the AH peptide-mediated vesicle-to-bilayer structural transformation on membrane surface charge, we plotted time-independent curves that describe changes in the adsorbed vesicle layer’s properties (Figure 2).
Figure 1. Influence of lipid composition on AH peptide-mediated structural transformation. Changes in (a) frequency and (b) energy dissipation as functions of time were tracked by QCM-D monitoring. Vesicle and peptide injection are indicated by the arrows labeled 1 and 2, respectively. A buffer wash was performed only after vesicle adsorption reached saturation.
Figure 2. Relative change in energy dissipation versus frequency for AH peptide-mediated structural transformation. Time-independent QCMD measurement curves describe the AH peptide-mediated, vesicle-tobilayer structural transformation in terms of adlayer properties.
1a and S1). The frequency shift is due to peptide adsorption onto the vesicles and also a previously reported increase in hydrodynamically coupled solvent.15 In addition, a key finding was that the magnitude of the frequency shift depended on the lipid composition. The most appreciable effect was observed with zwitteronic POPC vesicles, with a maximum change in frequency reaching −243 Hz (123% increase). Positively charged POPC:POEPC vesicles were also significantly affected by the binding interaction and, in this case, the maximum changes in frequency were approximately −210 Hz (93−104% increase). By contrast, negatively charged POPC:POPS vesicles were less affected and the maximum changes in frequency were less than −150 Hz (15−42% increase). As previously remarked, the observed frequency shfits are due to peptide uptake on the vesicle surface as well as a more appreciable uptake in hydrodynamically coupled solvent mass that accompanies vesicle destabilization. The increase in film hydration is also reflected in the corresponding increase in energy dissipation (Figures 1b and S2). Eventually, vesicle destabilization induced vesicle rupture, as reflected by the maximum change in frequency. In turn, AH peptide promoted a structural transformation of the adsorbed vesicle layer to form a planar bilayer. The final changes in the frequency and energy dissipation were approximately −26 Hz and less than 0.3 × 10−6, respectively (Table 1). These values are in agreement with previously reported values for planar bilayers, both from vesicle fusion experiments on silicon oxide4 as well as from AH peptide-mediated bilayer formation on gold and titanum oxide involving zwitterionic lipids only.11
Specifically, the curves present the relative change in QCM-D frequency versus energy dissipation throughout the vesicle-tobilayer structural transformation. The area inside the curve provides a qualitative indicator of the extent of change in adorbate film properties. Specifically, a greater area inside the curve is related to more extensive changes in film properties due to AH peptide. The zwitteronic POPC composition was most affected by the structural transformation, with a maximum change in energy dissipation reaching as high as 44.6 × 10−6 (810% increase). Similarly, positively charged POPC:POEPC compositions had large changes in energy dissipation of approximately 33 × 10−6 (713% increase). Although still significant, negatively charged POPC:POPS compositions were less affected, with maximum changes in energy disspation of less than 20 × 10−6 (392% increase or less). Overall, the results indicate that vesicle destabilization occurs more appreciably for zwitterionic compositions, as compared to charged lipid compositions. The viscoelastic properties of the adlayer throughout the structural transformation were also analyzed by the VoigtVoinova model (Figures S3,S4). As the change in frequency shows overtone-dependent behavior, the goal of the model fitting was to estimate the change in effective film thickness associated with the structural transformation. Specifically, a ratio was calculated in order to compare the maximum effective Voigt thickness versus the effective Voigt thickness of the adsorbed 3618
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process occurred the quickest for the 70:30 POPC:POPS composition and the slowest for the 70:30 POPC:POEPC composition. In between these two compositions (i.e., the most negatively and postively charged ones), there was a correlation between the time required for bilayer formation and membrane surface charge. In general, formation of negatively charged bilayers occurred more quickly than for other compositions. As the titanium oxide substrate is negatively charged,26 this finding was surprising because the bilayer formation process was fastest when there was the greatest electrostatic repulsion between vesicles and the substrate. Following this line of evidence, we also evaluated the time required for the vesicle-to-bilayer structural transformation (Figure 3b). We defined this time as corresponding to the lipid relaxation stage that lasts from when vesicle rupture becomes predominant (i.e., inflection point in the QCM-D frequency shift) until the planar bilayer is formed. If the post-rupture reassembly process is primarily affected by vesicle−substrate interactions, then it would be expected that the time required for the structural transformation is quickest for positively charged vesicles. However, this time measure was the fastest for negatively charged POPC:POPS vesicles and slowest for positively charged POPC:POEPC vesicles. Therefore, we may conclude that the kinetic differences related to membrane surface charge are not influenced primarily by the vesicle−substrate interaction. To further test the influence of membrane surface charge on AH peptide-mediated vesicle rupture, we performed ellipsometric measurements in order to quantify the amount of AH peptide bound to the adsorbed vesicle layers on titanium oxide (Figures 4 and S6). For the POPC and 70:30 POPC:POEPC
vesicle layer (Figure S5). The maximum thickness describes the extent of vesicle destabilization before rupture commences, and is related to the uptake in hydrodynamically coupled solvent that accompanies peptide binding. Hence, the ratio between the two values provides an indication of how greatly the adlayer properties were affected during the vesicle destabilization process. For zwitterionic POPC and positively charged POPC:POEPC compositions, the ratio was approximately between 2.5 and 3. By contrast, for negatively charged POPC:POPS compositions, the ratio was approximately 1.5. Taken together, the findings support that negatively charged vesicle adlayers require less vesicle destabilization in order for vesicle rupture to be induced. We also investigated the kinetics of the AH peptide-mediated bilayer formation process and identified trends related to the lipid composition. From peptide addition to complete bilayer formation, the overall duration lasted from 5 to 14 min, depending on the lipid composition (Figure 3a). On average, the
Figure 4. Optical mass tracking of AH peptide-mediated structral transformation. Ellipsometric measurements were performed in order to measure changes in the optical mass associated with the AH peptidemediated structural transformation. Figure 3. Kinetics of planar bilayer formation. Effect of lipid composition on the time required for (a) overall bilayer formation process from AH peptide addition until planar bilayer formation, and (b) post-rupture reassembly of ruptured vesicles to form a planar bilayer. Post-rupture is defined as the time corresponding to the lipid relaxation stage that lasts from vesicle rupture (maximum change in frequency) until the planar bilayer is formed (approximated as time at which the change in frequency reaches −30 Hz, as compared to the measurement baseline).
lipid compositions, there was an initial uptake in peptide mass before vesicle rupture commenced, as reflected by an inflection point in the maximum optical mass. By contrast, for the 70:30 POPC:POPS lipid composition, peptide uptake was not observed as a discrete step prior to vesicle rupture and accordingly there was no inflection point. Rather, it appears that AH peptide binding led to nearly immediate rupture of negatively charged vesicles because the optical mass quickly 3619
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decreased from ∼800 ng·cm−2 to ∼400 ng·cm−2. These findings support that negatively charged vesicles do not undergo appreciable vesicle fusion, but rather rupture directly. Furthermore, the optical mass of all resulting planar bilayers (∼400 ng·cm−2) confirms the QCM-D measurement results and supports that the bilayer formation process was complete. In order to explain the differences in AH peptide-mediated vesicle rupture as a function of membrane surface charge, it is notewothy that the rupture process can involve vesicle fusion events that are similar to classical vesicle fusion.15 Hence, vesicle−vesicle interactions are a key factor to explain the observed trends related to lipid composition. The most extensive structural rearrangement occurred for the zwitterionic POPC composition, which would have minimal electrostatic repulsion between vesicles. The least extensive structural rearrangement occurred for negatively charged POPC:POPS compositions, which would be expected to have the greatest electrostatic repulsion between vesicles. In particular, the POPS lipid bears a negatively charged carboxylic acid on its headgroup and contains three charges overall (two negative and one positive). By contrast, the POEPC lipid is an O-ethyl derivative of POPC with the only difference being that POEPC has an ethylated phosphate group.27 Hence, there is only one charge in the POEPC lipid and it is not exposed on the vesicle surface. This structural difference between POPS and POEPC lipids may explain why POPC:POEPC compositions undergo vesicle fusion more appreciably than POPC:POPS compositions. Concerning the kinetics of the process, it is important to note that lipid compositions which underwent significant vesicle destabilization and fusion took a longer time to form a planar bilayer. By contrast, POPC:POPS compositions had a relatively small structural rearrangement, and quickly formed planar bilayers. These differences suggest that mechanistic details in the vesicle-to-bilayer structural transformation may vary depending on the lipid composition. Presumably, AH peptide-induced membrane structural rearrangement is caused by asymmetric peptide adsorption onto the vesicle’s external leaflet and likely involves vesicle fusion in order to account for unbalanced membrane expansion.28 Due to electrostatic repulsion, POPC:POPS compositions are less able to accommodate vesicle fusion, so vesicle rupture is more favorable to address the unbalanced expansion. Based on the preferential rupture of negatively charged vesicles, it initially appears that AH peptide bears similarity to antimicrobial peptides which are also membrane-active agents.29 Indeed, antimicrobial peptides typically exhibit selectivity for lipid composition30 or membrane surface charge,31 with preference toward negatively charged lipid membranes. However, there is an important structural distinction between AH peptide and antimicrobial peptides in general. AH peptide has a zero net charge, whereas antimicrobial peptides are typically cationic. This difference may also explain why AH peptide is able to rupture lipid vesicles largely independent of membrane surface charge. In addition, the influence of lipid composition on AH peptide’s membranotropic activity supports its capability as a broadspectrum antiviral drug candidate. Indeed, AH peptide can target a wide range of enveloped viruses, including HIV, hepatitis C, dengue, and herpes simplex, by rupturing the lipid envelope.32 While virus size is one factor that helps explain AH peptide’s targeting range,13 the findings in this study demonstrate that lipid composition is another key parameter to evaluate. The
implications of these findings for antiviral medicine remain to be investigated in future work.
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CONCLUSION Herein, we have demonstrated that AH peptide is a versatile agent to rupture adsorbed vesicles with varying membrane surface charges. Starting from surface-adsorbed vesicle layers, we observed that AH peptide binding first induces vesicle destabilization and fusion prior to rupture for all tested compositions. However, there were important differences in the kinetics of the process. Negatively charged vesicles underwent less destabilization, as compared to positively charged and zwitterionic vesicles. This difference is likely due to the inability of negatively charged vesicles to fuse. In turn, bilayer formation from negatively charged lipid compositions was quickest despite electrostatic repulsion caused by the titanium oxide surface also being negatively charged. Collectively, the results show that AH peptide is able to promote bilayer formation from both negatively and positively charged lipid compositions, and it is therefore an attractive tool for model membrane fabrication. This capability is important because AH peptide can also promote bilayer formation on materials that are intractable to conventional vesicle fusion. Furthermore, the wide range of lipid compositions which are amenable to AH peptide’s membrane-targeting support its capability as a broad-spectrum antiviral drug candidate.
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ASSOCIATED CONTENT
S Supporting Information *
More detailed information is provided about QCM-D experimental analysis (Figures S1,S2), Voigt-Voinova model analysis (Figure S3−S5), and ellipsometry experiments (Figure S6). This material is available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Author Contributions
H. Z. Goh and J. A. Jackman contributed equally to this work. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS The authors wish to acknowledge support from the National Research Foundation (NRF-NRFF2011-01), the National Medical Research Council (NMRC/CBRG/0005/2012), and Nanyang Technological University to N.J.C. J.A.J. is a recipient of the Nanyang President’s Graduate Scholarship.
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REFERENCES
(1) Boxer, S. G. Molecular Transport and Organization in Supported Lipid Membranes. Curr. Opin. Chem. Biol. 2000, 4 (6), 704−709. (2) Sackmann, E. Supported Membranes: Scientific and Practical Applications. Science 1996, 271 (5245), 43−48. (3) Richter, R. P.; Bérat, R.; Brisson, A. R. Formation of SolidSupported Lipid Bilayers: An Integrated View. Langmuir 2006, 22 (8), 3497−3505. (4) Keller, C.; Kasemo, B. Surface Specific Kinetics of Lipid Vesicle Adsorption Measured with a Quartz Crystal Microbalance. Biophys. J. 1998, 75 (3), 1397−1402.
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(5) Reviakine, I.; Brisson, A. Formation of Supported Phospholipid Bilayers from Unilamellar Vesicles Investigated by Atomic Force Microscopy. Langmuir 2000, 16 (4), 1806−1815. (6) Czolkos, I.; Jesorka, A.; Orwar, O. Molecular Phospholipid Films on Solid Supports. Soft Matter 2011, 7 (10), 4562−4576. (7) Mashaghi, A.; Mashaghi, S.; Reviakine, I.; Heeren, R. M.; Sandoghdar, V.; Bonn, M. Label-Free Characterization of Biomembranes: From Structure to Dynamics. Chem. Soc. Rev. 2014, 43, 887− 900. (8) Hardy, G. J.; Nayak, R.; Zauscher, S. Model Cell Membranes: Techniques to Form Complex Biomimetic Supported Lipid Bilayers via Vesicle Fusion. Curr. Opin. Colloid Interface Sci. 2013, 18, 448−458. (9) Mager, M. D.; Almquist, B.; Melosh, N. A. Formation and Characterization of Fluid Lipid Bilayers on Alumina. Langmuir 2008, 24 (22), 12734−12737. (10) Reimhult, E.; Hook, F.; Kasemo, B. Vesicle Adsorption on SiO2 and TiO2: Dependence on Vesicle Size. J. Chem. Phys. 2002, 117 (16), 7401−7404. (11) Cho, N. J.; Cho, S. J.; Cheong, K. H.; Glenn, J. S.; Frank, C. W. Employing an Amphipathic Viral Peptide to Create a Lipid Bilayer on Au and TiO2. J. Am. Chem. Soc. 2007, 129 (33), 10050−10051. (12) Elazar, M.; Cheong, K. H.; Liu, P.; Greenberg, H. B.; Rice, C. M.; Glenn, J. S. Amphipathic Helix-Dependent Localization of NS5A Mediates Hepatitis C Virus RNA Replication. J. Virol. 2003, 77 (10), 6055−6061. (13) Cho, N. J.; Dvory-Sobol, H.; Xiong, A.; Cho, S. J.; Frank, C. W.; Glenn, J. S. Mechanism of an Amphipathic Alpha-Helical Peptide’s Antiviral Activity Involves Size-Dependent Virus Particle Lysis. ACS Chem. Biol. 2009, 4 (12), 1061−1067. (14) Cho, N.-J.; Frank, C. W.; Kasemo, B.; Höök, F. Quartz Crystal Microbalance with Dissipation Monitoring of Supported Lipid Bilayers on Various Substrates. Nat. Protoc. 2010, 5 (6), 1096−1106. (15) Cho, N. J.; Wang, G.; Edvardsson, M.; Glenn, J. S.; Hook, F.; Frank, C. W. Alpha-Helical Peptide-Induced Vesicle Rupture Revealing New Insight into the Vesicle Fusion Process as Monitored In Situ by Quartz Crystal Microbalance-Dissipation and Reflectometry. Anal. Chem. 2009, 81 (12), 4752−4761. (16) Tabaei, S. R.; Rabe, M.; Zhdanov, V. P.; Cho, N. J.; Höök, F. Single Vesicle Analysis Reveals Nanoscale Membrane Curvature Selective Pore Formation in Lipid Membranes by an Antiviral α-Helical Peptide. Nano Lett. 2012, 12 (11), 5719−5725. (17) Hardy, G. J.; Nayak, R.; Munir Alam, S.; Shapter, J. G.; Heinrich, F.; Zauscher, S. Biomimetic Supported Lipid Bilayers with High Cholesterol Content Formed by α-Helical Peptide-Induced Vesicle Fusion. J. Mater. Chem. 2012, 22 (37), 19506−19513. (18) Epand, R. M.; Vogel, H. J. Diversity of Antimicrobial Peptides and Their Mechanisms of Action. Biochim. Biophys. Acta 1999, 1462 (1), 11−28. (19) Felgner, P. L.; Ringold, G. Cationic Liposome-Mediated Transfection. Nature 1989, 337 (6205), 387−388. (20) MacDonald, R. C.; MacDonald, R. I.; Menco, B. P. M.; Takeshita, K.; Subbarao, N. K.; Hu, L.-r. Small-Volume Extrusion Apparatus for Preparation of Large, Unilamellar Vesicles. Biochim. Biophys. Acta 1991, 1061 (2), 297−303. (21) Cho, N.-J.; Kanazawa, K. K.; Glenn, J. S.; Frank, C. W. Employing Two Different Quartz Crystal Microbalance Models to Study Changes in Viscoelastic Behavior upon Transformation of Lipid Vesicles to a Bilayer on a Gold Surface. Anal. Chem. 2007, 79 (18), 7027−7035. (22) Voinova, M.; Jonson, M.; Kasemo, B. ‘Missing Mass’ Effect in Biosensor’s QCM Applications. Biosens. Bioelectron. 2002, 17 (10), 835−841. (23) Jackman, J. A.; Goh, H. Z.; Zhdanov, V. P.; Cho, N.-J. Rupture of Lipid Vesicles by a Broad-Spectrum Antiviral Peptide: Influence of Vesicle Size. J. Phys. Chem. B 2013, 117, 16117−16128. (24) Benes, M.; Billy, D.; Benda, A.; Speijer, H.; Hof, M.; Hermens, W. T. Surface-Dependent Transitions during Self-Assembly of Phospholipid Membranes on Mica, Silica, and Glass. Langmuir 2004, 20 (23), 10129−10137.
(25) De Feijter, J. a.; Benjamins, J.; Veer, F. a. Ellipsometry as a Tool to Study the Adsorption Behavior of Synthetic and Biopolymers at the AirWater Interface. Biopolymers 1978, 17, 1759−72. (26) Tero, R.; Ujihara, T.; Urisu, T. Lipid Bilayer Membrane with Atomic Step Structure: Supported Bilayer on a Step-and-Terrace TiO2 (100) Surface. Langmuir 2008, 24 (20), 11567−11576. (27) MacDonald, R. C.; Ashley, G. W.; Shida, M. M.; Rakhmanova, V. A.; Tarahovsky, Y. S.; Pantazatos, D. P.; Kennedy, M. T.; Pozharski, E. V.; Baker, K. A.; Jones, R. D. Physical and Biological Properties of Cationic Triesters of Phosphatidylcholine. Biophys. J. 1999, 77 (5), 2612−2629. (28) Woo, H.-J.; Wallqvist, A. Spontaneous Buckling of Lipid Bilayer and Vesicle Budding Induced by Antimicrobial Peptide Magainin 2: A Coarse-Grained Simulation Study. J. Phys. Chem. B 2011, 115 (25), 8122−8129. (29) Shai, Y. Mechanism of the Binding, Insertion and Destabilization of Phospholipid Bilayer Membranes by α-Helical Antimicrobial and Cell Non-Selective Membrane-Lytic Peptides. Biochim. Biophys. Acta 1999, 1462 (1), 55−70. (30) Huang, H. W. Action of Antimicrobial Peptides: Two-State Model. Biochemistry 2000, 39 (29), 8347−8352. (31) Tossi, A.; Sandri, L.; Giangaspero, A. Amphipathic, α-Helical Antimicrobial Peptides. Pept. Sci. 2000, 55 (1), 4−30. (32) Jackman, J. A.; Cho, N.-J. Model Membrane Platforms for Biomedicine: Case Study on Antiviral Drug Development. Biointerphases 2012, 7 (1−4), 1−20.
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